Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1976 Apr;256(2):361–379. doi: 10.1113/jphysiol.1976.sp011329

Short-term adaptive changes in the human vestibulo-ocular reflex arc

A Gonshor 1, G Melvill Jones 1
PMCID: PMC1309312  PMID: 16992507

Abstract

1. Two sets of experiments have examined the vestibulo-ocular response (VOR) to repeated sinusoidal rotation (A) in the dark and (B) after attempting visual tracking of a mirror-reversed image of the visual surround.

2. In both A and B a horizontal sinusoidal rotational stimulus of 1/6 Hz and 60°/sec angular velocity amplitude was employed, specifically chosen to lie within the presumed range of natural stimulation of the semicircular canals.

3. In A each of seven subjects underwent ten 2-min runs of the standard stimulus in the dark on each of three consecutive days, with 3-min rest periods between runs. Using d.c. electro-oculography (EOG) the VOR gain was measured throughout as eye velocity/head velocity. Mental arousal was maintained by competitive mental arithmetic. Constancy of EOG gain was assured by 50 min dark adaptation before experimentation.

4. The results of A showed no consistent change of VOR gain over the three times scales of a run, a day and the 3-day experiment.

5. In B the same subjects underwent a similar pattern of vestibular stimulation, but during eight of the 2-min daily runs they attempted the reversed visual tracking task. VOR gain was measured during the 1st, 6th and last runs which were conducted in the dark for this purpose. Constancy of EOG gain was maintained by using red light throughout.

6. The results of B showed a substantial (approx. 25%) and highly significant (P « 0·001) reduction of VOR gain attributable solely to the 16 min of reversed visual tracking attempted during the 50 min daily experiment. In addition the pre-test control gain was lower on day 3 than on day 1 (approx. 10% attenuation, P < 0·01) indicating a small cumulative effect from beginning to end of the 3-day experiment.

7. It is concluded (A) that the repeated vestibular stimulus did not itself cause significant attenuation of VOR gain, but (B) that superposition of a reversed visual tracking task did induce retained VOR attenuation which was solely due to the antagonistic visual stimulus.

8. In conjunction with other experimental evidence it is inferred that this attenuation probably represents an adaptive change in the VOR induced at least in part by retinal image slip.

Full text

PDF
361

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Angaut P., Brodal A. The projection of the "vestibulocerebellum" onto the vestibular nuclei in the cat. Arch Ital Biol. 1967 Nov;105(4):441–479. [PubMed] [Google Scholar]
  2. BRODAL A., HOIVIK B. SITE AND MODE OF TERMINATION OF PRIMARY VESTIBULOCEREBELLAR FIBRES IN THE CAT. AN EXPERIMENTAL STUDY WITH SILVER IMPREGNATION METHODS. Arch Ital Biol. 1964 Jan 8;102:1–21. [PubMed] [Google Scholar]
  3. Baker R., Precht W., Llinás R. Cerebellar modulatory action on the vestibulo-trochlear pathway in the cat. Exp Brain Res. 1972;15(4):364–385. doi: 10.1007/BF00234124. [DOI] [PubMed] [Google Scholar]
  4. COLLINS W. E., CRAMPTON G. H., POSNER J. B. Effects of mental activity on vestibular nystagmus and the electroencephalogram. Nature. 1961 Apr 8;190:194–195. doi: 10.1038/190194b0. [DOI] [PubMed] [Google Scholar]
  5. COLLINS W. E. Effects of mental set upon vestibular nystagmus. J Exp Psychol. 1962 Feb;63:191–197. doi: 10.1037/h0039941. [DOI] [PubMed] [Google Scholar]
  6. COLLINS W. E. PRIMARY, SECONDARY, AND CALORIC NYSTAGMUS OF THE CAT FOLLOWING HABITUATION TO ROTATION. J Comp Physiol Psychol. 1964 Jun;57:417–421. doi: 10.1037/h0044426. [DOI] [PubMed] [Google Scholar]
  7. Carpenter M. B., Stein B. M., Peter P. Primary vestibulocerebellar fibers in the monkey: distribution of fibers arising from distinctive cell groups of the vestibular ganglia. Am J Anat. 1972 Oct;135(2):221–249. doi: 10.1002/aja.1001350209. [DOI] [PubMed] [Google Scholar]
  8. Collins W. E. Special effects of brief periods of visual fixation on nystagmus and sensations of turning. Aerosp Med. 1968 Mar;39(3):257–266. [PubMed] [Google Scholar]
  9. Collins W. E., Updegraff B. P. A comparison of nystagmus habituation in the cat and the dog. Acta Otolaryngol. 1966 Jul;62(1):19–26. doi: 10.3109/00016486609119546. [DOI] [PubMed] [Google Scholar]
  10. Dichgans J., Brandt T. Visual-vestibular interaction and motion perception. Bibl Ophthalmol. 1972;82:327–338. [PubMed] [Google Scholar]
  11. Dix M. R., Hood J. D. Observations upon the nervous mechanism of vestibular habituation. Acta Otolaryngol. 1969 Feb-Mar;67(2):310–318. doi: 10.3109/00016486909125456. [DOI] [PubMed] [Google Scholar]
  12. FLUUR E., MENDEL L. Habituation, efference and vestibular interplay. I. Monaural caloric habituation. Acta Otolaryngol. 1962 Jul-Aug;55:65–80. doi: 10.3109/00016486209127340. [DOI] [PubMed] [Google Scholar]
  13. FLUUR E., MENDEL L. Habituation, efference and vestibular interplay. II. Combined caloric habituation. Acta Otolaryngol. 1962 Jul-Aug;55:136–144. doi: 10.3109/00016486209127346. [DOI] [PubMed] [Google Scholar]
  14. GUEDRY F. E., Jr PSYCHOPHYSIOLOGICAL STUDIES OF VESTIBULAR FUNCTION. Contrib Sens Physiol. 1965;14:63–135. doi: 10.1016/b978-1-4831-6746-6.50008-0. [DOI] [PubMed] [Google Scholar]
  15. Ghelarducci B., Ito M., Yagi N. Impulse discharges from flocculus Purkinje cells of alert rabbits during visual stimulation combined with horizontal head rotation. Brain Res. 1975 Apr 4;87(1):66–72. doi: 10.1016/0006-8993(75)90780-5. [DOI] [PubMed] [Google Scholar]
  16. Gonshor A., Jones G. M. Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol. 1976 Apr;256(2):381–414. doi: 10.1113/jphysiol.1976.sp011330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gonshor A., Malcolm R. Effect of changes in illumination level on electro-oculography (EOG). Aerosp Med. 1971 Feb;42(2):138–140. [PubMed] [Google Scholar]
  18. HALLPIKE C. S., HOOD J. D. Fatigue and adaptation of the cupular mechanism of the human horizontal semicircular canal: an experimental investigation. Proc R Soc Lond B Biol Sci. 1953 Sep;141(905):542–561. doi: 10.1098/rspb.1953.0060. [DOI] [PubMed] [Google Scholar]
  19. HOOD J. D., PFALTZ C. R. Observations upon the effects of repeated stimulation upon rotational and caloric nystagmus. J Physiol. 1954 Apr 28;124(1):130–144. doi: 10.1113/jphysiol.1954.sp005092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Henn V., Young L. R., Finley C. Vestibular nucleus units in alert monkeys are also influenced by moving visual fields. Brain Res. 1974 May 10;71(1):144–149. doi: 10.1016/0006-8993(74)90198-x. [DOI] [PubMed] [Google Scholar]
  21. Ito M., Highstein S. M., Fukuda J. Cerebellar inhibition of the vestibulo-ocular reflex in rabbit and cat and its blockage by picrotoxin. Brain Res. 1970 Feb 3;17(3):524–526. doi: 10.1016/0006-8993(70)90261-1. [DOI] [PubMed] [Google Scholar]
  22. Ito M. Neurophysiological aspects of the cerebellar motor control system. Int J Neurol. 1970;7(2):162–176. [PubMed] [Google Scholar]
  23. Ito M., Shiida T., Yagi N., Yamamoto M. Visual influence on rabbit horizontal vestibulo-ocular reflex presumably effected via the cerebellar flocculus. Brain Res. 1974 Jan 4;65(1):170–174. doi: 10.1016/0006-8993(74)90344-8. [DOI] [PubMed] [Google Scholar]
  24. JONES G. M., SPELLS K. E. A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc R Soc Lond B Biol Sci. 1963 Mar 26;157:403–419. doi: 10.1098/rspb.1963.0019. [DOI] [PubMed] [Google Scholar]
  25. Jones G. M., Milsum J. H. Characteristics of neural transmission from the semicircular canal to the vestibular nuclei of cats. J Physiol. 1970 Aug;209(2):295–316. doi: 10.1113/jphysiol.1970.sp009166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jones G. M., Milsum J. H. Frequency-response analysis of central vestibular unit activity resulting from rotational stimulation of the semicircular canals. J Physiol. 1971 Dec;219(1):191–215. doi: 10.1113/jphysiol.1971.sp009657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jones G. M., Milsum J. H. Spatial and dynamic aspects of visual fixation. IEEE Trans Biomed Eng. 1965 Apr;12(2):54–62. doi: 10.1109/tbme.1965.4502350. [DOI] [PubMed] [Google Scholar]
  28. Jones G. M. Transfer function of labyrinthine volleys through the vestibular nuclei. Prog Brain Res. 1972;37:139–156. doi: 10.1016/S0079-6123(08)63899-6. [DOI] [PubMed] [Google Scholar]
  29. Komatsuzaki A., Harris H. E., Alpert J., Cohen B. Horizontal nystagmus of rhesus monkeys. Acta Otolaryngol. 1969 May;67(5):535–551. doi: 10.3109/00016486909125481. [DOI] [PubMed] [Google Scholar]
  30. Lisberger S. G., Fuchs A. F. Response of flocculus Purkinje cells to adequate vestibular stimulation in the alert monkey: fixation vs. compensatory eye movements. Brain Res. 1974 Apr 5;69(2):347–353. doi: 10.1016/0006-8993(74)90013-4. [DOI] [PubMed] [Google Scholar]
  31. Llinás R., Precht W., Clarke M. Cerebellar Purkinje cell responses to physiological stimulation of the vestibular system in the frog. Exp Brain Res. 1971 Oct 25;13(4):408–431. doi: 10.1007/BF00234339. [DOI] [PubMed] [Google Scholar]
  32. MAYNE R. The dynamic characteristics of the semicircular canals. J Comp Physiol Psychol. 1950 Aug;43(4):309–319. doi: 10.1037/h0054827. [DOI] [PubMed] [Google Scholar]
  33. Maekawa K., Simpson J. I. Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system. J Neurophysiol. 1973 Jul;36(4):649–666. doi: 10.1152/jn.1973.36.4.649. [DOI] [PubMed] [Google Scholar]
  34. Mertens R. A., Collins W. E. Unilateral caloric habituation of nystagmus in the cat. Effects on rotational and bilateral caloric responses. Acta Otolaryngol. 1967 Oct;64(4):281–297. doi: 10.3109/00016486709139117. [DOI] [PubMed] [Google Scholar]
  35. Miles F. A., Fuller J. H. Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey. Brain Res. 1974 Nov 22;80(3):512–516. doi: 10.1016/0006-8993(74)91035-x. [DOI] [PubMed] [Google Scholar]
  36. SHACKEL B. Pilot study in electro-oculography. Br J Ophthalmol. 1960 Feb;44:89–113. doi: 10.1136/bjo.44.2.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shimazu H., Smith C. M. Cerebellar and labyrinthine influences on single vestibular neurons identified by natural stimuli. J Neurophysiol. 1971 Jul;34(4):493–508. doi: 10.1152/jn.1971.34.4.493. [DOI] [PubMed] [Google Scholar]
  38. VAN EGMOND A. A. J., GROEN J. J., JONGKEES L. B. W. The mechanics of the semicircular canal. J Physiol. 1949 Dec 15;110(1-2):1–17. doi: 10.1113/jphysiol.1949.sp004416. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES